Segment-specific adhesion as a driver of convergent extension.
Convergent extension, the simultaneous extension and narrowing of tissues, is a crucial event in the formation of the main body axis during embryonic development. It involves processes on multiple scales: the sub-cellular, cellular and tissue level, which interact via explicit or intrinsic feedback...
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Public Library of Science (PLoS)
2015-02-01
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| Series: | PLoS Computational Biology |
| Online Access: | https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1004092&type=printable |
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| author | Renske M A Vroomans Paulien Hogeweg Kirsten H W J ten Tusscher |
| author_facet | Renske M A Vroomans Paulien Hogeweg Kirsten H W J ten Tusscher |
| author_sort | Renske M A Vroomans |
| collection | DOAJ |
| description | Convergent extension, the simultaneous extension and narrowing of tissues, is a crucial event in the formation of the main body axis during embryonic development. It involves processes on multiple scales: the sub-cellular, cellular and tissue level, which interact via explicit or intrinsic feedback mechanisms. Computational modelling studies play an important role in unravelling the multiscale feedbacks underlying convergent extension. Convergent extension usually operates in tissue which has been patterned or is currently being patterned into distinct domains of gene expression. How such tissue patterns are maintained during the large scale tissue movements of convergent extension has thus far not been investigated. Intriguingly, experimental data indicate that in certain cases these tissue patterns may drive convergent extension rather than requiring safeguarding against convergent extension. Here we use a 2D Cellular Potts Model (CPM) of a tissue prepatterned into segments, to show that convergent extension tends to disrupt this pre-existing segmental pattern. However, when cells preferentially adhere to cells of the same segment type, segment integrity is maintained without any reduction in tissue extension. Strikingly, we demonstrate that this segment-specific adhesion is by itself sufficient to drive convergent extension. Convergent extension is enhanced when we endow our in silico cells with persistence of motion, which in vivo would naturally follow from cytoskeletal dynamics. Finally, we extend our model to confirm the generality of our results. We demonstrate a similar effect of differential adhesion on convergent extension in tissues that can only extend in a single direction (as often occurs due to the inertia of the head region of the embryo), and in tissues prepatterned into a sequence of domains resulting in two opposing adhesive gradients, rather than alternating segments. |
| format | Article |
| id | doaj-art-9e85bf1f38c64924bd0237f83099d5ef |
| institution | DOAJ |
| issn | 1553-734X 1553-7358 |
| language | English |
| publishDate | 2015-02-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Computational Biology |
| spelling | doaj-art-9e85bf1f38c64924bd0237f83099d5ef2025-08-20T03:01:35ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582015-02-01112e100409210.1371/journal.pcbi.1004092Segment-specific adhesion as a driver of convergent extension.Renske M A VroomansPaulien HogewegKirsten H W J ten TusscherConvergent extension, the simultaneous extension and narrowing of tissues, is a crucial event in the formation of the main body axis during embryonic development. It involves processes on multiple scales: the sub-cellular, cellular and tissue level, which interact via explicit or intrinsic feedback mechanisms. Computational modelling studies play an important role in unravelling the multiscale feedbacks underlying convergent extension. Convergent extension usually operates in tissue which has been patterned or is currently being patterned into distinct domains of gene expression. How such tissue patterns are maintained during the large scale tissue movements of convergent extension has thus far not been investigated. Intriguingly, experimental data indicate that in certain cases these tissue patterns may drive convergent extension rather than requiring safeguarding against convergent extension. Here we use a 2D Cellular Potts Model (CPM) of a tissue prepatterned into segments, to show that convergent extension tends to disrupt this pre-existing segmental pattern. However, when cells preferentially adhere to cells of the same segment type, segment integrity is maintained without any reduction in tissue extension. Strikingly, we demonstrate that this segment-specific adhesion is by itself sufficient to drive convergent extension. Convergent extension is enhanced when we endow our in silico cells with persistence of motion, which in vivo would naturally follow from cytoskeletal dynamics. Finally, we extend our model to confirm the generality of our results. We demonstrate a similar effect of differential adhesion on convergent extension in tissues that can only extend in a single direction (as often occurs due to the inertia of the head region of the embryo), and in tissues prepatterned into a sequence of domains resulting in two opposing adhesive gradients, rather than alternating segments.https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1004092&type=printable |
| spellingShingle | Renske M A Vroomans Paulien Hogeweg Kirsten H W J ten Tusscher Segment-specific adhesion as a driver of convergent extension. PLoS Computational Biology |
| title | Segment-specific adhesion as a driver of convergent extension. |
| title_full | Segment-specific adhesion as a driver of convergent extension. |
| title_fullStr | Segment-specific adhesion as a driver of convergent extension. |
| title_full_unstemmed | Segment-specific adhesion as a driver of convergent extension. |
| title_short | Segment-specific adhesion as a driver of convergent extension. |
| title_sort | segment specific adhesion as a driver of convergent extension |
| url | https://journals.plos.org/ploscompbiol/article/file?id=10.1371/journal.pcbi.1004092&type=printable |
| work_keys_str_mv | AT renskemavroomans segmentspecificadhesionasadriverofconvergentextension AT paulienhogeweg segmentspecificadhesionasadriverofconvergentextension AT kirstenhwjtentusscher segmentspecificadhesionasadriverofconvergentextension |